These Plants Change colour When Exposed to a Pesticide

Thanks to some genetic tricks, plants can now speak in colour. A team of researchers at the University of California, Riverside hacked the natural stress response system in Arabidopsis thaliana, a small white-flowered plant from the mustard family that serves as a common model organism in plant biology labs. When exposed to the pesticide azinphos-ethyl, A. thaliana turns from green to red, flagging the contamination loud and clear.

“It’s an unambiguous readout of what’s in the environment,” says Ian Wheeldon, co-lead researcher and a UC Riverside chemical engineering professor. He believes that giving plants the power to share what they’re experiencing, in a way that’s visible to the naked eye, will deepen people’s understanding of them.

The idea of using plants as environmental sentinels isn’t new. Years ago, plant biologists noticed that trinitrotoluene (TNT, an explosive) builds up in root tissues, choking plants. Researchers succeeded in growing plants that could detect TNT in the soil, but signaling that information to people was complicated. In 2016, biologists at MIT figured out how to make them glow in infrared light in front of a camera attached to a computer, which could then send an email alert.

There are lower-tech methods of confirming whether a plant was exposed to contaminants, like bringing samples back to a lab for testing, but that can be costly and time-consuming. Sensors in the field can track things like light levels, soil conditions, and moisture, but they still require a power source—which will eventually require maintenance or shut down entirely.

Getting plants to simply change colour would be much easier. “This technique is nice because you don’t need any special equipment. You just see it,” says Yunde Zhao, a professor of cell and developmental biology at the University of California, San Diego who was not involved in this project.

This study, published last week in Nature Chemical Biology, is the first to use a visible marker to detect organophosphate pesticides in plants. Sophisticated synthetic biology tools, enabling researchers to turn on gene expression in response to specific environmental triggers, already exist for biological systems like human cell lines and bacteria—single-celled organisms with short life cycles. “In plants, those tools are very limited,” says co-lead researcher and UC Riverside plant biologist Sean Cutler.

Manipulating molecular pathways in complex multicellular plants that take months to grow is much trickier than running experiments in microbes, where a scientist can make a genetic tweak and observe the consequences in a single sitting. With this project, the team aimed to scale these tools up, “building the widgets that allow us to program lots of complicated inputs and outputs in a plant system,” Cutler says.

The team engineered the plants to respond to the pesticide azinphos-ethyl, which has been banned in the European Union because of its toxicity in mammals. They did this by hijacking a hormonal pathway that plants use to signal distress.

Arabidopsis, like all plants, uses a hormone called abscisic acid, or ABA, to send alerts when it’s stressed by conditions like cold, drought, or changes in soil chemistry. ABA binds to receptors in the plant, making it close its pores to hold in more water. Cutler’s team rewired this pathway by changing the shape of the ABA receptor’s binding pocket, molding it so it can also detect and bind to azinphos-ethyl molecules.

Binding something other than ABA to an ABA receptor could trigger the plant’s stress response, but that isn’t easy for people to see without special equipment and close observation. So the researchers wanted the molecular binding to make the plant do something visibly obvious: change colour.

To make A. thaliana turn red on cue, the researchers gave the plants a gene from beets. They used a long synthetic DNA sequence developed by Zhao’s lab called RUBY, which contains instructions for making betalain, the bright red pigment that gives beets their signature colour. When exposed to this pesticide, their engineered compound acts as a sensor, activating RUBY. As a result, the plant’s leaves turn from green to deep red. “The results are just beautiful,” says Zhao.

“This paper is opening up a new capacity to reprogram plant responses,” says Stanford bioengineering professor Jenn Brophy, who was not involved in the study. But she points out that this kind of engineering gets tricky—a tiny change to a protein’s structure can change how it folds, causing it to malfunction. The team needed to make sure the ABA receptor could sense the pesticide but still be able to perform its usual job.

Cutler says his team found specific protein mutations that they harnessed to make a system where the individual pieces couldn’t interfere with the plant’s normal signaling pathways. “Part A is broken on its own, and part B is broken on its own,” he says. “But magically, when they’re together, their function is restored.”

Theoretically, one could make a plant turn red in response to any number of chemicals, not just azinphos-ethyl. Many organophosphate pesticides are chemically similar enough to bind to the same modified receptor. But making the plant respond differently to each chemical—like blue for acephate and purple for malathion—is much harder. With every additional pathway, the odds of metabolism-disrupting cross talk get higher.

The signal doesn’t necessarily have to be a visible colour change—the team has also experimented with temperature. A second receptor pathway in these engineered plants responds to diazinon, an insecticide that’s currently banned for residential use in the United States. As part of the same study, the team used diazinon to turn on the plant’s normal ABA signaling, triggering a stress-induced increase in leaf temperature that can be seen by infrared night-vision cameras, similar to what the MIT team had tried before.

The challenge now is figuring out just how many molecular switches can be engineered before things get too complicated—and creating separate pathways that all produce easily observable outputs. Wheeldon believes it will be worth the effort. Having more switches, he says, “increases the complexity of the questions you can answer and the applications you can go after.”

While these colour-changing plants still only exist in the lab, Cutler says his team hopes to “create biosensors that allow you to engineer organisms that sense all kinds of chemicals.” For example, because plants already produce ABA in response to drought; he imagines thirsty plants that could change colour overnight to call for help before they experience real damage.

Wheeldon’s research group has been studying pesticides for years—they’re used in agriculture globally, so they were an obvious first target for sensing experiments. But Cutler’s team has a long list of molecules that they’re testing now: pharmaceuticals, substances of abuse, natural plant products, and other agrochemicals.

“In the long run, I think that we will be able to create biotechnologies that can help provide the public or other specific users with information on chemicals in the environment,” says Wheeldon. “Real-time feedback about what is in the environment—for example, is the local water supply contaminated? Are bad actors using harmful chemicals in their industrial processes?”

Brophy envisions at-home applications for this technology too, for the black thumbs amongst us, like “houseplants that change colours to tell you that they need something.”

“I feel a lot of pressure to have nice plants in my office, being a professor of plant biology. But oh man, I just struggle,” she says, chuckling.

Because these plants are transgenic—meaning they contain DNA from another species—they would face a tough approval process if anyone tried to bring them to market in the US. Betalain-producing plants and A. thaliana don’t naturally cross-pollinate, so researchers would need to demonstrate that any transgenic plant they engineer won’t have any unintended effects on the environment.

It’s not impossible, though. Earlier this year, the US Department of Agriculture approved the sale of purple tomatoes, which contain snapdragon genes that boost their antioxidant content and increase shelf life. Last month, the agency gave the go-ahead to a glow-in-the-dark petunia that contains genes from bioluminescent mushrooms and will go to market next year.

With more research, plants that speak in colour may get the green light too.

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